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Phage Therapy As a Potential Solution in the Fight Against ARTICLE https://doi.org/10.1057/s41599-020-0478-4 OPEN Phage therapy as a potential solution in the fight against AMR: obstacles and possible futures ✉ Charlotte Brives 1 & Jessica Pourraz2 ABSTRACT Phage therapy, the use of bacteriophage viruses to treat bacterial infections, has existed for more than a hundred years. However, the practice is struggling to develop, despite growing support over the past 15 years from researchers and doctors, who see it as a 1234567890():,; promising therapy in the context of the rise of antimicrobial resistance (AMR). While the reasons for these developmental difficulties are complex, in this article we wish to address the effects of pharmaceutical regulations on phage therapy. By showing how phages are assimilated to an umpteenth antibiotic in legal texts, but also in certain medical practices, this article proposes to analyze the consequences of such regulatory categorization both for their production and the logistics of administration of proof of their efficacy in randomized con- trolled trials (RCTs), as well as the underlying concepts of infection and treatment. This paper follows Chandler’s work on the concept of antibiotics as infrastructure and its inversion presented by antimicrobial resistance. Phages as living, dynamic, evolving, and specific entities, do not lend themselves easily to current categories, norms, and development models. In this sense, they act as disruptors, revealing the limitations imposed by the existing infrastructure. More precisely here, and to continue Chandler’s initial thought process, this paper aims to show that antibiotics also form a kind of epistemological infrastructure, which acts as a powerful inhibitor to the development of phage therapy. In this sense antibiotics prevent the development of solutions to the problem they contribute to create. But the difficulties phage therapy faces, as highlighted in this article, can be interpreted as entry points for thinking of another medicine and imagining other possible futures. This analysis is based on a 3-year fieldwork study (2016–2019) in Europe (France, Belgium, and Switzerland), during which we conducted semi-directed interviews with various phage therapy stake- holders (physicians, researchers, pharmacists, regulators, patients, and patient associations), participatory observation in labs and observations during symposia and workshops on phages and phage therapy. ✉ 1 CNRS, Bordeaux, France. 2 Faculté de Sociologie, Université de Bordeaux, Bordeaux, France. email: [email protected] PALGRAVE COMMUNICATIONS | (2020) 6:100 | https://doi.org/10.1057/s41599-020-0478-4 | www.nature.com/palcomms 1 ARTICLE PALGRAVE COMMUNICATIONS | https://doi.org/10.1057/s41599-020-0478-4 Introduction hage therapy, the use of bacteriophage viruses to treat the materiality of phages, evolving entities, imposes constraints bacterial infections, has existed for more than a hundred on both the respect of production norms imposed by regulations P ’ years (D Hérelle, 1931). However, the practice is struggling and the dominant model of drug development based on to develop, despite growing support over the past 15 years from scalability. researchers and doctors, who see it as a promising therapy in the After a brief review of the history of phage therapy and the context of the rise of antimicrobial resistance (AMR). While the mode of action of phages, we will describe the regulations in force reasons for these developmental difficulties are complex, in this in Europe, which classify bacteriophage viruses as medicinal article we wish to address the effects of pharmaceutical regula- products and their use, particularly in the French context. tions on phage therapy. For this we have adopted a theoretical By showing how phages are assimilated to an umpteenth approach from science and technology studies (STS) and philo- antibiotic in legal texts, but also in certain medical practices, we sophy of science. More precisely, we use the material-semiotic will analyze the consequences of such regulatory categorization method of the actor-network theory, and the principle of gen- for their production and for the administration of proof of their eralized symmetry that places humans and non-humans on the efficacy in randomized controlled trials (RCTs), as well as the same analytical plane (Callon, 1986; Latour, 2004). Our postulate underlying concepts of infection and treatment. is that we cannot understand the difficulties of phage therapy We will conclude with how some of the difficulties facing without taking into account both the socio-political context and phage therapy highlighted in this article can be interpreted as the very materiality of phages, their characteristics and entry points for imagining other possible futures. specificities. This analysis is informed by 3 years of fieldwork (2016–2019). Indeed, efforts to make phage therapy a viable and widely shared As one of us is a member of various scientific networks on phage practice must be analyzed within the framework of the AMR research and applications, and has trained in Biological Sciences, problem and the solutions proposed to deal with it (Podolsky, Anthropology of Science and Biomedical Sciences, she was able to 2018). More broadly, while the need to reduce antibiotic use by conduct participatory observations in laboratory contexts. We modulating individual behaviors is often highlighted (Broom et al., participated as observers in 10 symposia and workshops on 2015), it is the systemic and institutionalized dimension of anti- bacteriophages and phage therapy, during which we conducted biotics and their use that must be taken into account to understand intensive informal discussions with participants. We also con- how a new practice may or may not emerge. ducted 30 semi-directive and/or open interviews with scientists, The development of antibiotics, but above all of their modes of physicians, pharmacists, patients, start-up actors and regulatory production (Bud, 2009) and of mass-consumption, in both agency officers.1 As anthropologists, we are also part of a Ran- human and animal health (Hinchliffe et al., 2018; Kirchhelle, domized Controlled Trial, the aim of which is to assess the added 2018; Fortané, 2019), have had a profound and lasting impact on value of phages for bone infections. both human societies and bacteria, thus reminding us that the These different implications within the phage therapy field latter are not inert matter, but living organisms that act and react meant one of us could participate to a specialized committee on to their environment (Landecker, 2016). phage therapy at the French National Agency for the Safety of In a 2018 article, Chandler proposes to mobilize the notion of Medicines and Health Products (ANSM). From a strong inter- “infrastructure” as developed by Bowker and Star (1999), among disciplinary perspective, we also presented our work in work- others, as an analytical and programmatic framework to under- shops on phage therapy and in a Jacques Monod conference on stand the question of AMR: “Such infrastructure comprises viral evolution, generating added conversations and data about materials, information, ordering. For example, the availability and actors’ perspectives on the development of phage therapy. usability of research instruments and subjects shapes what science is constructed; the supply chain, techniques, and subject handling methods are invented alongside biology’s conceptual frame” A brief history of phage therapy (Chandler, 2018, p. 9). Chandler shows how “the present Not all viruses are pathogenic to humans. In fact, there is a awareness of antimicrobial resistance appears to have produced category of virus, bacteriophage viruses (or phages), which are an inversion whereby antimicrobials, and their attendant rela- hosted by bacteria. The human population will soon reach eight tions and processes, have come to the fore. This enables analyses billion, but the number of phages present in ecosystems is esti- of the possibilities, conventions, and constraints that have mated at more than 1031, making them the most represented hitherto been taken for granted as common sense, and the biological entity on Earth. These creatures, made up of protein or potential for reshaping these into the future” (Chandler, 2018). proteolipidic capsides containing fragments of nucleic acids (most This inversion of the infrastructure presented by AMR, and the often DNA, but also RNA), are present wherever bacteria can opportunity it offers to think of another medicine, seems to us to be be found. particularly highlighted by the case of phage therapy. Phages, living Humans have come to know and recognize them since the and dynamic, evolving and specific entities, do not lend themselves beginning of the 20th century. First mentioned in 1915 by Fre- easily to current categories, norms and development models. In this derick Twort (1915), they owe their therapeutic applications to sense, they are disruptors, revealing the limitations imposed by the Félix d’Hérelle, who isolated them in 1917 in the feces of con- existing infrastructure. More precisely here, rather than reinvesting valescing dysentery patients, while he was stationed at the Pasteur the various forms of the antibiotic infrastructure through the prism Institute in Paris (D’Hérelle, 1917). of phages, something that cannot be achieved in a single article, we Though the nature of the bacteriophages was a matter of dis- want to show that antibiotics also form a kind of epistemological pute only resolved
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